Resilience and stability of the CF- intestinal and respiratory microbiome during nutritional and exercise intervention

Abstract Background Impaired respiratory and intestinal microbiome composition is linked to cystic fibrosis lung disease severity. In people with cystic fibrosis (pwCF), regular exercise is recommended to delay disease progression and preserve a stable lung function. An optimal nutritional status is...

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Main Authors: Rebecca L. Knoll, Víctor Hugo Jarquín-Díaz, Jonas Klopp, Alissa Kemper, Katja Hilbert, Barlo Hillen, Daniel Pfirrmann, Perikles Simon, Viola Bähner, Oliver Nitsche, Stephan Gehring, Lajos Markó, Sofia K. Forslund, Krystyna Poplawska
Format: Article
Language:English
Published: BMC 2023-02-01
Series:BMC Microbiology
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Online Access:https://doi.org/10.1186/s12866-023-02788-y
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author Rebecca L. Knoll
Víctor Hugo Jarquín-Díaz
Jonas Klopp
Alissa Kemper
Katja Hilbert
Barlo Hillen
Daniel Pfirrmann
Perikles Simon
Viola Bähner
Oliver Nitsche
Stephan Gehring
Lajos Markó
Sofia K. Forslund
Krystyna Poplawska
author_facet Rebecca L. Knoll
Víctor Hugo Jarquín-Díaz
Jonas Klopp
Alissa Kemper
Katja Hilbert
Barlo Hillen
Daniel Pfirrmann
Perikles Simon
Viola Bähner
Oliver Nitsche
Stephan Gehring
Lajos Markó
Sofia K. Forslund
Krystyna Poplawska
author_sort Rebecca L. Knoll
collection DOAJ
description Abstract Background Impaired respiratory and intestinal microbiome composition is linked to cystic fibrosis lung disease severity. In people with cystic fibrosis (pwCF), regular exercise is recommended to delay disease progression and preserve a stable lung function. An optimal nutritional status is vital for best clinical outcomes. Our study investigated whether regular and monitored exercise and nutritional support promotes CF microbiome health. Methods A personalized nutrition and exercise program promoted nutritional intake and physical fitness in 18 pwCF for 12 months. Throughout the study, patients performed strength and endurance training monitored by a sports scientist via an internet platform. After three months, food supplementation with Lactobacillus rhamnosus LGG was introduced. Nutritional status and physical fitness were assessed before the study started, after three and nine months. Sputum and stool were collected, and microbial composition was analyzed by 16S rRNA gene sequencing. Results Sputum and stool microbiome composition remained stable and highly specific to each patient during the study period. Disease-associated pathogens dominated sputum composition. Lung disease severity and recent antibiotic treatment had the highest impact on taxonomic composition in stool and sputum microbiome. Strikingly, the long-term antibiotic treatment burden had only a minor influence. Conclusion Despite the exercise and nutritional intervention, respiratory and intestinal microbiomes proved to be resilient. Dominant pathogens drove the composition and functionality of the microbiome. Further studies are required to understand which therapy could destabilize the dominant disease-associated microbial composition of pwCF.
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spelling doaj.art-4940f5d6cda94a86b8d3cac094e0c2cd2023-03-22T10:34:32ZengBMCBMC Microbiology1471-21802023-02-0123111210.1186/s12866-023-02788-yResilience and stability of the CF- intestinal and respiratory microbiome during nutritional and exercise interventionRebecca L. Knoll0Víctor Hugo Jarquín-Díaz1Jonas Klopp2Alissa Kemper3Katja Hilbert4Barlo Hillen5Daniel Pfirrmann6Perikles Simon7Viola Bähner8Oliver Nitsche9Stephan Gehring10Lajos Markó11Sofia K. Forslund12Krystyna Poplawska13Pediatric Pulmonology, Allergology and Cystic Fibrosis, Children’s Hospital, University Medical Center of the Johannes Gutenberg-University MainzExperimental and Clinical Research Center, a cooperation between the Max Delbrück Center for Molecular Medicine in the Helmholtz Association and Charité Universitätsmedizin BerlinPediatric Immunology and Infectiology, Children’s Hospital, University Medical Center of the Johannes Gutenberg-University MainzPediatric Pulmonology, Allergology and Cystic Fibrosis, Children’s Hospital, University Medical Center of the Johannes Gutenberg-University MainzPediatric Immunology and Infectiology, Children’s Hospital, University Medical Center of the Johannes Gutenberg-University MainzDepartment of Sports Medicine, Prevention, and Rehabilitation, Faculty of Social Science, Media and Sports, Johannes Gutenberg-University MainzDepartment of Sports Medicine, Prevention, and Rehabilitation, Faculty of Social Science, Media and Sports, Johannes Gutenberg-University MainzDepartment of Sports Medicine, Prevention, and Rehabilitation, Faculty of Social Science, Media and Sports, Johannes Gutenberg-University MainzPediatric Pulmonology, Allergology and Cystic Fibrosis, Children’s Hospital, University Medical Center of the Johannes Gutenberg-University MainzPediatric Pulmonology, Allergology and Cystic Fibrosis, Children’s Hospital, University Medical Center of the Johannes Gutenberg-University MainzPediatric Immunology and Infectiology, Children’s Hospital, University Medical Center of the Johannes Gutenberg-University MainzExperimental and Clinical Research Center, a cooperation between the Max Delbrück Center for Molecular Medicine in the Helmholtz Association and Charité Universitätsmedizin BerlinExperimental and Clinical Research Center, a cooperation between the Max Delbrück Center for Molecular Medicine in the Helmholtz Association and Charité Universitätsmedizin BerlinPediatric Pulmonology, Allergology and Cystic Fibrosis, Children’s Hospital, University Medical Center of the Johannes Gutenberg-University MainzAbstract Background Impaired respiratory and intestinal microbiome composition is linked to cystic fibrosis lung disease severity. In people with cystic fibrosis (pwCF), regular exercise is recommended to delay disease progression and preserve a stable lung function. An optimal nutritional status is vital for best clinical outcomes. Our study investigated whether regular and monitored exercise and nutritional support promotes CF microbiome health. Methods A personalized nutrition and exercise program promoted nutritional intake and physical fitness in 18 pwCF for 12 months. Throughout the study, patients performed strength and endurance training monitored by a sports scientist via an internet platform. After three months, food supplementation with Lactobacillus rhamnosus LGG was introduced. Nutritional status and physical fitness were assessed before the study started, after three and nine months. Sputum and stool were collected, and microbial composition was analyzed by 16S rRNA gene sequencing. Results Sputum and stool microbiome composition remained stable and highly specific to each patient during the study period. Disease-associated pathogens dominated sputum composition. Lung disease severity and recent antibiotic treatment had the highest impact on taxonomic composition in stool and sputum microbiome. Strikingly, the long-term antibiotic treatment burden had only a minor influence. Conclusion Despite the exercise and nutritional intervention, respiratory and intestinal microbiomes proved to be resilient. Dominant pathogens drove the composition and functionality of the microbiome. Further studies are required to understand which therapy could destabilize the dominant disease-associated microbial composition of pwCF.https://doi.org/10.1186/s12866-023-02788-yCystic fibrosisMicrobiomeGut-lung axisPhysical exerciseNutritionAntibiotics
spellingShingle Rebecca L. Knoll
Víctor Hugo Jarquín-Díaz
Jonas Klopp
Alissa Kemper
Katja Hilbert
Barlo Hillen
Daniel Pfirrmann
Perikles Simon
Viola Bähner
Oliver Nitsche
Stephan Gehring
Lajos Markó
Sofia K. Forslund
Krystyna Poplawska
Resilience and stability of the CF- intestinal and respiratory microbiome during nutritional and exercise intervention
BMC Microbiology
Cystic fibrosis
Microbiome
Gut-lung axis
Physical exercise
Nutrition
Antibiotics
title Resilience and stability of the CF- intestinal and respiratory microbiome during nutritional and exercise intervention
title_full Resilience and stability of the CF- intestinal and respiratory microbiome during nutritional and exercise intervention
title_fullStr Resilience and stability of the CF- intestinal and respiratory microbiome during nutritional and exercise intervention
title_full_unstemmed Resilience and stability of the CF- intestinal and respiratory microbiome during nutritional and exercise intervention
title_short Resilience and stability of the CF- intestinal and respiratory microbiome during nutritional and exercise intervention
title_sort resilience and stability of the cf intestinal and respiratory microbiome during nutritional and exercise intervention
topic Cystic fibrosis
Microbiome
Gut-lung axis
Physical exercise
Nutrition
Antibiotics
url https://doi.org/10.1186/s12866-023-02788-y
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